The role of multiple wildlife hosts in the persistence and spread of bovine tuberculosis in New Zealand.

AIM: To explore how the inclusion of multi-host dynamics affects the predicted prevalence of bovine tuberculosis (TB) in possums and other host species following the current best practice for control of TB in large difficult and remote areas, to identify which host species are responsible for changes in predicted prevalence, and whether TB can persist in possum-free host communities. METHODS: Multi-host TB models were constructed, comprising three host species with density-dependent population growth, density-dependent disease transmission and susceptible and infected classes. Models were parameterised for two case studies of current concern in New Zealand, namely chronic TB persistence in a possum-deer-pig complex in extensive forest, and in a possum-pig-ferret complex in unforested semi-arid shrub and grasslands. Persistence of TB in the face of best practice possum control was evaluated from model simulations, and the contribution of different hosts to persistence of TB was assessed by removing each host species in turn from the simulations. A sensitivity test explored how different parameter values affected modelled persistence of TB. RESULTS: The forest multi-host model-predicted amplification of TB prevalence due to the presence of pigs. The presence of pigs and/or deer did not jeopardise the success of best practice possum control in eradicating TB from the system, as pigs and deer are effectively end-hosts for TB. Sensitivity analyses indicated these interpretations were robust to uncertainty in model parameter values. The grassland system model predicted that the multi-host species complex could potentially lead to failure of eradication of TB under possum-only control, due to TB persisting in ferret and pig populations in the absence of possum hosts through reciprocal scavenging, resulting in spillback transmission to possums once their populations had started to recover from control. CONCLUSIONS: With respect to management of TB, for modelled forest habitats, 15 years of effective possum control was predicted to eradicate TB from the possum-deer-pig host community, indicating the current focus on possum-only control is appropriate for such areas. For grassland model systems, TB was predicted to persist in the ferret-pig host complex in the absence of possums, potentially jeopardising the effectiveness of possum-only control programmes. However this outcome depended on the occurrence and rate of pigs acquiring TB from ferrets, which is unknown. Thus some estimation of this transmission parameter is required to enable managers to assess if multi-host disease dynamics are important for their TB control programmes.

Development of integrated surveillance systems for the management of tuberculosis in New Zealand wildlife.

Disease surveillance for the management of bovine tuberculosis (TB) in New Zealand has focussed, to a large extent, on the development of tools specific for monitoring Mycobacterium bovis infection in wildlife. Diagnostic techniques have been modified progressively over 30 years of surveillance of TB in wildlife, from initial characterisation of gross TB lesions in a variety of wildlife, through development of sensitive culture techniques to identify viable mycobacteria, to molecular identification of individual M. bovis strains. Of key importance in disease surveillance has been the elucidation of the roles that different wildlife species play in the transmission of infection, specifically defining brushtail possums (Trichosurus vulpecula) as true maintenance hosts compared to those that are predominantly spillover hosts, but which may serve as useful sentinel species to indicate TB persistence. Epidemiological modelling has played a major role in TB surveillance, initially providing the theoretical support for large-scale possum population control and setting targets at which control effort should be deployed to ensure disease eradication. As TB prevalence in livestock and wildlife declined throughout the 2000s, more varied field tools were developed to gather surveillance data from the diminishing possum populations, and to provide information on changing TB prevalence. Accordingly, ever more precise (but disparate) surveillance information began to be integrated into multi-faceted decision-assist models to support TB management decisions, particularly to provide informed parameters at which control effort could be halted, culminating in the Proof of Freedom modelling framework that now allows an area to be declared TB-free within chosen confidence limits. As New Zealand moves from large-scale TB control to regional eradication of disease in the coming years, further integrative models will need to be developed to support management decisions, based on combined field data of possum and TB prevalence, sentinel information, risk assessment in relation to financial benefits, and changing political and environmental needs.

A novel approach to assess the probability of disease eradication from a wild-animal reservoir host.

Surveying and declaring disease freedom in wildlife is difficult because information on population size and spatial distribution is often inadequate. We describe and demonstrate a novel spatial model of wildlife disease-surveillance data for predicting the probability of freedom of bovine tuberculosis (caused by Mycobacterium bovis) in New Zealand, in which the introduced brushtail possum (Trichosurus vulpecula) is the primary wildlife reservoir. Using parameters governing home-range size, probability of capture, probability of infection and spatial relative risks of infection we employed survey data on reservoir hosts and spillover sentinels to make inference on the probability of eradication. Our analysis revealed high sensitivity of model predictions to parameter values, which demonstrated important differences in the information contained in survey data of host-reservoir and spillover-sentinel species. The modelling can increase cost efficiency by reducing the likelihood of prematurely declaring success due to insufficient control, and avoiding unnecessary costs due to excessive control and monitoring.

Oral vaccination reduces the incidence of tuberculosis in free-living brushtail possums.

Bovine tuberculosis (Tb) caused by Mycobacterium bovis has proved refractory to eradication from domestic livestock in countries with wildlife disease reservoirs. Vaccination of wild hosts offers a way of controlling Tb in livestock without wildlife culling. This study was conducted in a Tb-endemic region of New Zealand, where the introduced Australian brushtail possum (Trichosurus vulpecula) is the main wildlife reservoir of Tb. Possums were trapped and vaccinated using a prototype oral-delivery system to deliver the Tb vaccine bacille Calmette-Guerin. Vaccinated and control possums were matched according to age, sex and location, re-trapped bimonthly and assessed for Tb status by palpation and lesion aspiration; the site was depopulated after 2 years and post-mortem examinations were conducted to further identify clinical Tb cases and subclinical infection. Significantly fewer culture-confirmed Tb cases were recorded in vaccinated possums (1/51) compared with control animals (12/71); the transition probability from susceptible to infected was significantly reduced in both males and females by vaccination. Vaccine efficacy was estimated at 95 per cent (87-100%) for females and 96 per cent (82-99%) for males. Hence, this trial demonstrates that orally delivered live bacterial vaccines can significantly protect wildlife against natural disease exposure, indicating that wildlife vaccination, along with existing control methods, could be used to eradicate Tb from domestic animals.

Protection of free-living and captive possums against pulmonary challenge with Mycobacterium bovis following oral BCG vaccination.

In New Zealand, possums (Trichosurus vulpecula) are the main wildlife reservoir for bovine tuberculosis (Tb), which they transmit to livestock. This study investigated oral vaccination with lipid-formulated Mycobacterium bovis BCG and subsequent protection against virulent M. bovis challenge in wild-caught possums. Possums were trapped from the field and either hand-vaccinated and released back into the wild, or acclimatised to captive conditions prior to voluntary uptake of flavoured vaccine. Possums were subsequently exposed to pulmonary challenge with virulent M. bovis, administered either by instillation of a liquid suspension as an intra-tracheal challenge (field animals) or in micro-droplets as an aerosol (captive animals). Field studies indicated that the relative risk of death in wild possums due to Tb was 2.4 times greater in control compared with orally-vaccinated possums, with the vaccine conferring protection to possums in both good and poor body condition. Laboratory studies indicated that oral vaccination conferred protection in cage-acclimatised possums, with >3log(10) reduction in lung bacterial burdens among vaccinated animals. This study provides evidence that lipid-formulated BCG oral vaccine can provide significant protection to possums in field as well as laboratory conditions, which may favour the use of this formulation as a delivery method for controlling wildlife Tb.

The effect of fertility control on the transmission of bovine tuberculosis in wild brushtail possums.

AIM: To determine the effect of fertility control on the rate of transmission of bovine tuberculosis (Tb), caused by Mycobacterium bovis, in brushtail possums (Trichosurus vulpecula). METHODS: At two study sites with a history of Tb infection in the resident possum population, a sample of adult male and female possums (n=50), determined by palpation to be Tb-free, was surgically sterilised by gonadectomy. A sample of untreated Tb-free male and female possums (n=54) served as controls. Each study site was trapped every 2 months over a 3-year period, and the Tb status of the individuals in the trial assessed. At the conclusion of the trial, all remaining experimental individuals were killed, necropsied and examined for characteristic lesions typical of Tb. The rate of transmission of Tb infection was estimated using the incidence of tuberculous cases in the experimental animals and comparing it between sites, sex and sterilisation treatment. RESULTS: Sterilisation by gonadectomy resulted in a reduction in the rate of transmission of Tb in male possums by 53%, but a corresponding increase in sterilised females for reasons that are still unclear. However, this interaction was statistically weak (p=0.10). When the sexes were combined, there was no overall effect of sterilisation on the rate of transmission of Tb (p=0.43). Sterility treatment notwithstanding, there was a highly significant difference in the rate of transmission between the sexes (p=0.01), being almost one order of magnitude higher in untreated males compared with untreated females. CONCLUSIONS: Although lacking strong statistical support, these results suggest that fertility control that targets endocrine control of fertility may provide some additional benefits for disease control over that achieved by reductions in population density, by reducing the rate of transmission of M. bovis in male possums. However, additional studies are needed to confirm the validity of these results. The large difference in the rate of transmission of M. bovis in untreated males compared with untreated females suggests that transmission of Tb among males may be an important driver of the dynamics of Tb infection in possums.

Advances in understanding disease epidemiology and implications for control and eradication of tuberculosis in livestock: the experience from New Zealand.

A deteriorating tuberculosis problem in cattle and deer in New Zealand has been halted and then reversed over the last decade. Mycobacterium bovis infection in both wild and domestic animal populations has been controlled. This has been achieved by applying a multi-faceted science-based programme. Key features of this have been a comprehensive understanding of the epidemiology of tuberculosis in animals, confidence in sampling wild animal populations, effective application of diagnostic tests in cattle and deer, and the ability to map M. bovis genotypes.